Grass and

Forage Science

The Journal of the British Grassland Society The Official Journal of the European Grassland Federation

Changes in macro- and micronutrient contents of

grasses and forbs following Miscanthus x giganteus
feedstock, hydrochar and biochar application to
temperate grassland
S. Schimmelpfennig*, C. Kammann*, G. Moser*, L. Gr
unhage* and C. M
uller*,
*Institute for Experimental Plant Ecology, JLU Giessen, Giessen, Germany, School of Biology and
Environmental Science, University College Dublin, Dublin, Ireland

Abstract
Biochar and hydrochar application to soil holds promise for climate change mitigation. This study provides
first insights into the nutrient concentration and
removal of grassland vegetation after addition of various carbon compounds together with pig slurry. Four
treatments: control (no carbon application), feedstock,
hydrochar and biochar from Miscanthus x giganteus
were applied at a permanent grassland site near Giessen, Germany. Changes in plant functional groups,
biomass production and nutrition status were monitored over 2 years. Total biomass production was not
affected by the carbon amendments. However, biochar
favoured growth of forbs over grasses, while legume
growth was increased by all carbon amendments. The
initial nutrient concentrations of the carbon compounds were enriched according to their degree of
carbonization, potentially providing nutrients to
plants. The plant biomass from hydro- and biochar
amended plots, added up over 2 years, exhibited
higher potassium concentrations compared to biomass
from feedstock and control plots. All carbon amendments led to lower sodium concentrations in total biomass, compared to the control. Uncarbonized
feedstock led to increased manganese concentrations
in total biomass, while the concentrations of all other
heavy metals were not influenced by any carbon
amendment, compared to the control. From a plant
and animal nutritional point of view, none of the carbon amendments reduced grassland yield or fodder

Correspondence to: S. Schimmelpfennig, Institute for Experimental Plant Ecology, JLU Giessen, Heinrich-Buff-Ring
26-32, 35390 Giessen, Germany.
E-mail: sonja.schimmelpfennig@bot2.bio.uni-giessen.de
Received 22 July 2014; Accepted 15 December 2014

doi: 10.1111/gfs.12158

quality. The study suggests that hydrochar and, even

more so, biochar may provide a source of potassium
to plants.
Keywords: biochar, hydrochar, plant growth, grassland,
plant nutrients, nutrient concentration

Introduction
Carbon amendments such as hydrochar and biochar
are currently being studied as an option for climate
change mitigation (IPCC, 2007; Woolf et al., 2010),
with positive side effects on physico-chemical as well
as biological soil properties (Lehmann et al., 2006;
Atkinson et al., 2010; Titirici, 2013). Depending on
feedstock and process production conditions, biochar
was found to improve the nutrient status of the
amended soil directly by its nutrient content (Chan
and Xu, 2009), direct or indirect pH effects (Hossain
et al., 2011; Lehmann et al., 2011), or impacts on soil
nutrient cycling due to biocharfertilizer surface interactions (Clough et al., 2013). Two meta-studies on the
effect of biochar on plant growth revealed an overall
positive influence, with yield increases of 1012%
(Jeffery et al., 2011; Biederman and Harpole, 2013),
largely depending on the plant species. In contrast,
hydrochar has often proved to be detrimental to plant
growth and germination, even generating genotoxic
effects, assumedly due to N-limitation or labile carbon
fractions attached to the hydrochar as residues from
the production process (Gajic and Koch, 2012; Bargmann et al., 2013; Busch et al., 2013; Wagner and
Kaupenjohann, 2014).
Results on the long-term effects of carbon amendments on the soilplant matrix in temperate soils are
still scarce (Mukherjee and Lal, 2014). The opportunities for biochar to create soils of high fertility require

2015 John Wiley & Sons Ltd. Grass and Forage Science

S. Schimmelpfennig et al.

more attention (Ponomarenko and Anderson, 2001).

As most of the worlds grasslands are grazed and thus
receive a continuous supply of nutrients from animal
faeces, possible interactions of animal manure/urine
and carbon amendments need to be identified. Biochar reportedly reduced NH
3 losses from urine patches
in grazed land and from slurry during storage, possibly
due to reversible sorption mechanisms, providing a
nitrogen source to plants (Haeni et al., 2012; Taghizadeh-Toosi et al., 2012). Thus, the main aim of this
study was to identify the effects of three different carbon amendments on the plant nutrient composition of
grassland undergoing repeated slurry fertilization
(Scurlock and Hall, 1998). We hypothesized that feedstock and hydrochar would lead to a plant growth
reduction due to nitrogen limitation and we expected
biochar to have positive effects on plant nutrient
availability due to bonding of nutrients from slurry on
the biochar surface.

Materials and methods

We analysed the effect of Miscanthus x giganteus chaff
(uncarbonized = feedstock, hydrothermally carbonized
at 200C for 2 h = hydrochar and pyrolysed in a continuous flow reactor at 550600C = biochar) on the
plant biomass and its nutrient concentrations from
temperate grassland. A grassland field experiment had
been installed in Linden-Leihgestern, near Giessen
(50320 N, 841.30 E, at 172 m a.s.l.) in spring 2011.
The N-limited, extensively managed grassland (Haplic
Stagnosol: 25% sand, 28% clay, 47% silt and 36%
soil organic carbon) with an annual mean precipitation of 586 mm and a mean air temperature of 96C
(19972004) had received no fertilizer since 1993
(Janze, 2006). For more information on the site, see
Jager et al. (2003).
In the experiment, the carbon amendments were
applied in four random repetitions (4 9 4 m) as top
dressing (see also Schimmelpfennig et al. 2014). The
substrates were applied to achieve equal carbon
amendment (+20% of soil organic carbon, as calculated for the upper 10 cm of the soil with a bulk density of 1 g cm3) for all treatments except the control,
leading to an application of 16 kg m2 feedstock,
145 kg m2 hydrochar and 093 kg m2 biochar.
After the initiation of the experiment, the plots were
fertilized with pig slurry twice a year (control = no
Miscanthus amendment, normal slurry amendment).
The N-amounts given with the slurry were
536 + 210 kg N ha1 in 2011, 1100 + 567 kg N
ha1 in 2012 and 607 + 636 kg N ha1 in 2013
(spring and autumn respectively).
Plant biomass was cut twice a year (spring and
autumn) from three predefined harvest subplots

(60 9 60 cm) per plot, sorted by plant functional

groups (grasses, forbs and legumes), dried, quantified
and ground to 1 mm (SM 300; Retsch GmbH, Haan,
Germany). The three samples from the harvest subplots were pooled to one sample per plot and plant
functional group (grasses/forbs) for further analysis.
Legumes were not considered for analysis of trace elements and minerals because they accounted for only
13% on average of total biomass, providing not
enough material for analysis. Likewise, plant biomass
from 2011 was not sufficient for the analysis. This
resulted in n = 64 for grasses and forbs, and
grasses + forbs respectively (16 samples per season per
group). The single grass and forb species are provided
in Table 1.
Biomass carbon (C) and nitrogen (N) concentrations were analysed using an elemental analyser
(Vario Max, Hanau, Germany). For the analysis of
phosphorus (P), potassium (K), sulphur (S), calcium
(Ca), magnesium (Mg), iron (Fe), manganese (Mn),
copper (Cu), zinc (Zn), sodium (Na) and chlorine
(Cl), the plant samples were pressed in a ring vessel
to produce a pellet which was then dried to a residual moisture of <3% in 34 h at 60C before X-ray
fluorescence analysis. The analysis was carried out
by the Hessian Federal Laboratory, accredited by
the German National Accreditation Body in 2013.
The measurement procedure is validated by ring
trials, including 40 laboratories across Europe to
approve the reference material; see Table 2 for
illustration of detection limit, range limit and measurement uncertainty.
Initial macro- and micronutrient contents of hydrochar and biochar were determined using wet chemistry and atomic emission spectrometry after pressure
digestion by nitric acid and hydrogen peroxide. Miscanthus x giganteus feedstock was analysed with the plant
material as described above (Table 3). Soil pH values
(in H2O) were determined yearly from three pooled
samples per plot (030 cm).
Statistics were performed using SigmaPlot 11.0 and
IBM 20. Effects on biomass yield (dry matter), macroand microelement concentration and removal were
determined by a four-factorial univariate ANOVA, followed by post hoc tests (Tukeys HSD, CI = 95%)
where plant functional group (grasses/forbs), harvest
year (2012/2013), harvest season (spring/autumn),
plot replication (1, 2, 3, 4) and treatments (control,
feedstock, hydrochar and biochar) were modelled as
factors. Normal distribution of the residues was tested
by a KolmogorovSmirnov test with Lilliefors correction of significance. Differences in the N:P ratio due to
C-treatment were determined by a one-way ANOVA.
Differences in nutrient removal according to the plant
functional groups grasses and forbs were determined

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

Table 1 List of single grass, forb and legume species in the grassland under study.
Grasses
Arrhenaterium elatius
Alopecurus pratensis
Agrostis capillaris
Anthoxanthum odoratum
Avena pubescens
Dactylis glomerata
Deschampsia cespitosa
Festuca pratensis
Festuca rubra
Holcus lanatus
Lolium perenne
Luzula campestris
Phleum pratense
Poa pratensis
Poa trivialis
Trisetum flavescens

Forbs

Legumes

Achillea millefolium
Ajuga reptans
Anthriscus sylvestris
Bellis perennis
Campanula rotundifolia
Centaurea jacea
Cerastium holosteoides
Cirsium oleraceum
Crepis biennis
Filipendula ulmaria
Galium mollugo
Galium verum
Geranium pratensis
Glechoma hederacea
Leontodon autumnalis
Leucanthemum vulgare
Lysimachia nummularia
Myosotis arvensis
Plantago lanceolata
Ranunculus acris
Ranunculus repens
Rumex acetosa
Sanguisorba officinalis
Saxifraga granulata
Sensecio jacobae
Stellaria graminea
Taraxacum officinalis
Veronica chamaedris

Lathyrus pratensis
Lotus corniculatus
Medicago lupulina
Trifolium pratensis
Trifolium repens
Vicia cracca
Vicia sepium
Lathyrus pratensis
Lotus corniculatus
Medicago lupulina
Trifolium pratensis
Trifolium repens
Vicia cracca
Vicia sepium

by t-tests. If data were not normally distributed, we

log-10-transformed the data to achieve normal distribution. If unsuccessful, medians were tested with the
MannWhitney U median test. Correlations between
the nutrient concentrations of the carbon amendments
and the harvested biomass were tested using Pearson
productmoment correlations.
The nutrient use efficiency was determined by calculating the individual nutrient-to-C ratio (g/g) of the
samples (Chapin III et al., 2011). For evaluation of the
fodder quality of the plant biomass, measured nutrient
concentrations (g or mg kg1 respectively) were compared with the recommended intake as well as minimal requirements of micro- and macronutrients as
given by the German Agricultural Society (DLG) (Flachowsky et al., 2001), and values from reference grassland, taken from the DLG database (mean values of
available data n = 304, from German grassland 1935
2014). Differences between the experimental biomass
in this study and the values from the reference grassland from the DLG table were determined by one-way
ANOVAs.

2015 John Wiley & Sons Ltd. Grass and Forage Science

Results
Macro- and microelement contents of the carbon substrates generally increased with degree of carbonization (feedstock < hydrochar < biochar) (Table 3). Total
biomass dry matter (DM) (g m2) increased significantly from 2012 to 2013 (7260 vs. 8398 g m2,
P < 0001, n = 64, Figure 1a and b) but did not differ
with treatments. Nevertheless, we found significant
treatment effects over the 2 years in the biomass of
the plant functional groups grasses (P < 0001,
n = 64), forbs (P < 0001, n = 64) and legumes
(P = 0006, n = 64) (Figure 1c). Grass biomass was
highest in the control plots and lowest in the biochar
plots (67 vs. 50% of the total yield) and vice versa for
the forbs (31 vs. 47% of the total yield). All carbon
amendments led to an increased growth of legumes
(P = 0006, n = 64). The results of the biomass yield
remained unchanged if tested without legumes (no
treatment differences in the grass + forb yield).
The concentration of macro- and microelements
(in % and mg kg1) in the biomass differed according

Carbon amendment to temperate grassland

Figure 4 Mean air temperature in 2 m (C) and precipitation (mm) of the experimental site in the years 2012 and 2013.

Discussion
Plant functional group effects
The higher nutrient concentrations generally observed
in the forbs, compared to grasses, throughout all
treatments (Figure 2a and b) may possibly be
explained by an improved nutrient retention capability of forbs. This is common for nutrient-poor environments (Berendse et al., 1992; Aerts, 1999), as
defined by biomass N concentrations <15% (Maynard et al., 1976; Whitehead, 2000; G
usewell, 2004),
a threshold which was barely exceeded by the biomass harvested in our experiment, and a N:P ratio
<14 (Koerselman and Meuleman, 1996; Leuschner
and Ellenberg, 2010) which, with an average of 49,
has clearly occurred. Moreover, the nutrient needs
and uptakes of forbs, e.g. for Ca and Mg, are generally up to five times higher than that of grasses
(Bergmann, 1992).
Potassium, Mn and Cl concentrations were higher
in the grass biomass, when compared to forbs. For K,
the uptake from soil by plants seems to be a function
of root morphology, especially root length and surface
area in the topsoil (Schenk and Barber, 1980; Mengel
and Steffens, 1985). Thus, a reason for significantly

2015 John Wiley & Sons Ltd. Grass and Forage Science

higher K concentrations in the grass biomass could be

a higher fine and fibrous root density in the surface
layer of the soil, compared to forbs (Kutschera and
Lichtenegger, 1982; Sun et al., 1997; Kutschera et al.,
2009).
Grasses have been found to contain more Mn than
legumes in other experiments, and Mn uptake by
plants can vary substantially according to plant species
and site (Garmo et al., 1986; Bergmann, 1992; Lindstr
om et al., 2013). Nevertheless, in general, site variations, with varying soil properties such as pH values,
were found to have a greater impact on Mn uptake
than plant species and plant functional groups (Hemingway, 1962; Wagner and Kaupenjohann, 2014). In
our experiment, effects of soil pH on the release of
Mn seem unlikely as there were no treatment effects
on soil pH over the experimental period.
To our knowledge, there are no previous reports
on higher Cl uptake by grasses when compared to forbs. Differences in Cl concentration among the plant
groups, grasses and forbs, may also be explained by
differences in the abundance of fine and main roots as
well as root depth.
Significant effects of biochar amendment on biomass composition have been reported elsewhere (Van

Carbon amendment to temperate grassland

higher in 2012. This may be explained by an earlier

start of the growth period in 2013 and/or a cumulative fertilization effect (Figure 4). Increased biomass
growth together with lower biomass N concentrations
in 2013, but constant nutrient removal by the plants,
points to a dilution effect, also described as a Piper
Steenbjerg effect (Wikstr
om, 1994). The same effect
could possibly also apply to Mg with a constant nutrient removal but improved plant growth and hence
lower nutrient concentrations, indicating that Mg
availability triggered plant growth. Low Mg concentrations of the grass biomass (023%, half the concentration of the forbs) together with an improved grass
biomass growth in 2013 underline this assumption,
especially for grasses (Figures 1 and 2a, b).
A decreasing nutrient concentration, accompanied
by lower nutrient removals and increasing biomass
from 2012 to 2013, was found for P, K, S, Cu and
Cl, pointing to a suboptimal nutrient supply, especially in 2013. Nevertheless, these nutrients were not
growth limiting, and the higher biomass in 2013 was
accompanied by a better nutrient use efficiency in
this year. A positive linear relationship between concentrations, biomass growth and nutrient removal
was only found for Fe, indicating a sufficient nutrient
supply. Iron concentrations in the biomass were in
line with the average Fe contents of plants
(50200 mg kg1), although the total iron content
may not serve as the best criterion for the Fe status
of plant biomass (Bergmann, 1992). Ca and Mn concentrations were similar in 2012 and 2013, accompanied by constant nutrient removal and higher
nutrient use efficiency due to increased biomass
growth for Ca and constant nutrient use efficiency
and an increased removal in the case of Mn. This
indicates that for these elements, the dilution effect
does not apply, but neither was optimum supply
attained. Sodium concentrations and removals were
constant over both years, indicating that these elements were not limiting.

Treatment effects
Macronutrients: nitrogen, phosphorus, potassium,
sulphur, magnesium and calcium
In general, removal and concentration of N in the biomass was not influenced by any carbon amendment,
compared to the control plots, indicating that either
the carbon amendments had no N-limiting effect, as
was reported from other studies with Miscanthus straw
(Eiland et al., 2001) or sugar beet/wheat straw hydrochar (Gajic and Koch, 2012; Bargmann et al., 2014),
or more N that could be immobilized was added with
the slurry. Nevertheless, we observed a grass biomass

2015 John Wiley & Sons Ltd. Grass and Forage Science

13

growth reduction in the hydrochar-amended plots in

2011, the year of application, that was likely caused
by initial N-immobilization or phytotoxic effects (Bargmann et al., 2013; Busch et al., 2013). However, as the
results presented here show, this short-term effect was
outbalanced in the following years. Higher biomass N
concentrations due to biochar + N-fertilizer application
to soil, as found in incubation experiments (Chan
et al., 2008; Van Zwieten et al., 2010; Schimmelpfennig et al., 2014), were not observed, likely because the
biochar was not directly mixed into the soil matrix
due to top dressing. Moreover, biochars0 beneficial role
in soil nitrogen cycling might not be the decisive factor in soils with a naturally high nitrifier activity, as in
the grassland used here (Kammann et al., 1998; DeLuca et al., 2006).
Potassium concentrations were increased in all
carbon-amended plots, and correlated with the initial
K concentrations of the materials, indicating a fertilization effect. Removal of K was only higher in
hydrochar- and biochar-amended plots, compared to
the control (Figure 3). The difference was made up
mostly by the higher share of forbs in these plots,
confirming the promotion of forb over grass biomass
growth by the carbon amendments (Figures 1 and
5a). Potassium has been found to be easily leached
from biochar, thereby providing fertilizer to plants
(Gaskin et al., 2010; Silber et al., 2010; Yao et al.,
2010; Angst and Sohi, 2013; Wagner and
Kaupenjohann, 2014). Likewise, K from hydrochar is
reportedly plant available (Gajic and Koch, 2012)
and water soluble (Wagner and Kaupenjohann,
2014). A long-term K fertilization effect due to carbon amendment has been described as unlikely
(Angst and Sohi, 2013), but has also been found in
a natural grass system (Van de Voorde et al., 2013).
Besides the direct fertilization effect, the sorption of
K from slurry by negatively charged functional
groups on the biochar/hydrochar surface could also
be a reason for improved K availability in our experiment (Sevilla and Fuertes, 2009; Mukherjee et al.,
2011).
Both Ca and Mg contents were concentrated by
the hydrothermal carbonization and pyrolysis process,
compared to the feedstock material; nevertheless, the
nutrient amounts applied with all carbon amendments
were quite low, but were highest with hydrochar
amendment (78 g m2) (Table 3). Similar Ca and Mg
concentrations of the biomass from carbon-amended
plots, combined with a higher nutrient removal, are
likely due to the overall higher share of forbs in the
carbon-amended plots in the total biomass for the
2 years, compared to the control (Figures 1 and 5a).
The higher Ca and Mg removal in the hydrochar plots,
compared to the control plots, indicates that Ca and

S. Schimmelpfennig et al.

(a)

Figure 2 Mean macronutrient (a) and micronutrient (b) concentrations of the biomass dry matter (DM), sorted by treatment
(control, feedstock, hydrochar, biochar), season (spring/autumn), plant functional group (grasses/forbs) and year (2012/2013),
n = 64. Significant differences within the several factors, as determined by UNIANOVA, are given in the graphs.

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

(b)

Figure 2 continued.

2015 John Wiley & Sons Ltd. Grass and Forage Science

S. Schimmelpfennig et al.

Figure 3 Mean weighted concentrations of the macro- and micronutrients in % or mg kg1 biomass dry matter (DM) (biomass
yield and composition were considered). Letters mark significant differences between the treatments (n = 64).

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

Figure 4 Mean air temperature in 2 m (C) and precipitation (mm) of the experimental site in the years 2012 and 2013.

Discussion
Plant functional group effects
The higher nutrient concentrations generally observed
in the forbs, compared to grasses, throughout all
treatments (Figure 2a and b) may possibly be
explained by an improved nutrient retention capability of forbs. This is common for nutrient-poor environments (Berendse et al., 1992; Aerts, 1999), as
defined by biomass N concentrations <15% (Maynard et al., 1976; Whitehead, 2000; G
usewell, 2004),
a threshold which was barely exceeded by the biomass harvested in our experiment, and a N:P ratio
<14 (Koerselman and Meuleman, 1996; Leuschner
and Ellenberg, 2010) which, with an average of 49,
has clearly occurred. Moreover, the nutrient needs
and uptakes of forbs, e.g. for Ca and Mg, are generally up to five times higher than that of grasses
(Bergmann, 1992).
Potassium, Mn and Cl concentrations were higher
in the grass biomass, when compared to forbs. For K,
the uptake from soil by plants seems to be a function
of root morphology, especially root length and surface
area in the topsoil (Schenk and Barber, 1980; Mengel
and Steffens, 1985). Thus, a reason for significantly

2015 John Wiley & Sons Ltd. Grass and Forage Science

higher K concentrations in the grass biomass could be

a higher fine and fibrous root density in the surface
layer of the soil, compared to forbs (Kutschera and
Lichtenegger, 1982; Sun et al., 1997; Kutschera et al.,
2009).
Grasses have been found to contain more Mn than
legumes in other experiments, and Mn uptake by
plants can vary substantially according to plant species
and site (Garmo et al., 1986; Bergmann, 1992; Lindstr
om et al., 2013). Nevertheless, in general, site variations, with varying soil properties such as pH values,
were found to have a greater impact on Mn uptake
than plant species and plant functional groups (Hemingway, 1962; Wagner and Kaupenjohann, 2014). In
our experiment, effects of soil pH on the release of
Mn seem unlikely as there were no treatment effects
on soil pH over the experimental period.
To our knowledge, there are no previous reports
on higher Cl uptake by grasses when compared to forbs. Differences in Cl concentration among the plant
groups, grasses and forbs, may also be explained by
differences in the abundance of fine and main roots as
well as root depth.
Significant effects of biochar amendment on biomass composition have been reported elsewhere (Van

10

S. Schimmelpfennig et al.

(a)

Figure 5 Mean macronutrient (a) and micronutrient (b) removals (g m2) of the 2 years 2012 and 2013, shown for the different
treatment plots with standard deviation (n = 64). Different capital and lower case letters mark significant differences in nutrient
removal by grasses and forbs respectively. Greek letters mark significant differences of the overall biomass removal (grasses + forbs).

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

11

(b)

Figure 5 continued.
de Voorde et al., 2013) with legumes benefiting most
from an improved availability of P, K and higher pH
values due to biochar amendment, whereas the abundance of forbs was not affected.

2015 John Wiley & Sons Ltd. Grass and Forage Science

Dilution effects and nutrient use efficiency

Total harvested biomass increased from 2012 to 2013
by an average 113 g m2, although fertilization was

30  06

31  06

Hydrochar mean

Biochar mean

29  07
234  93

30  06

Feedstock mean

051

164  45
(+61%)
167  42
(+64%)
177  49
(+74%)
185  44
(+82%)
3

33  07

Minimal
requirement
Grass biomass
(German
Agricultural
Society Table)

1015

355

K
(g kg
DM1)

Recommended
intake
Control mean

P
(g kg
DM1)

55  24

88  21
(+53%)
91  20
(+58%)
92  16
(+60%)
89  15
(+55%)
061

575

Ca
(g kg
DM1)

20  08

31  07
(+94%)
29  06
(+81%)
30  04
(+94%)
29  05
(+81%)
05

16

Mg
(g kg
DM1)

n/s

17  03

17  03

18  02

18  03

12

S
(g kg
DM1)

1657  1056
(+235%)
1793  1522
(+259%)
1876  988
(+275%)
1824  1308
(+265%)
n/s

50

Fe
(mg kg1
DM)

05  06

03

02  01

02  01

03  01

04  02

14

Na (g kg
DM1)

789  293

1100  512
(+120%)
1457  849
(+191%)
1005  528
(+101%)
944  427
(+89%)
n/s

50

Mn
(mg kg1
DM)

72  19

77  24

75  22

77  23

80  27

810

Cu
(mg kg1
DM)

383  117

20

438  77

475  64

471  66

441  115

50

Zn
(mg kg1
DM)

78  21
(+132%)
76  20
(+134%)
74  18
(+121%)
74  17
(+121%)
n/s

335

Cl (g kg
DM1)

Table 4 Comparison of the recommended nutrient supply of a dairy cow with a mean performance of 30 kg milk per day and a daily intake of 20 kg biomass DM (German
Society of Nutritional Physiology) with the nutrient contents of the biomass from the treatment plots in the field experiment. For a further comparison, long-term mean values
from German grasslands (German Agricultural Society Fodder Quality Table, 19362014) are displayed. Numbers in brackets give the relative increase in % compared to the
recommended intake values.

12
S. Schimmelpfennig et al.

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

higher in 2012. This may be explained by an earlier

start of the growth period in 2013 and/or a cumulative fertilization effect (Figure 4). Increased biomass
growth together with lower biomass N concentrations
in 2013, but constant nutrient removal by the plants,
points to a dilution effect, also described as a Piper
Steenbjerg effect (Wikstr
om, 1994). The same effect
could possibly also apply to Mg with a constant nutrient removal but improved plant growth and hence
lower nutrient concentrations, indicating that Mg
availability triggered plant growth. Low Mg concentrations of the grass biomass (023%, half the concentration of the forbs) together with an improved grass
biomass growth in 2013 underline this assumption,
especially for grasses (Figures 1 and 2a, b).
A decreasing nutrient concentration, accompanied
by lower nutrient removals and increasing biomass
from 2012 to 2013, was found for P, K, S, Cu and
Cl, pointing to a suboptimal nutrient supply, especially in 2013. Nevertheless, these nutrients were not
growth limiting, and the higher biomass in 2013 was
accompanied by a better nutrient use efficiency in
this year. A positive linear relationship between concentrations, biomass growth and nutrient removal
was only found for Fe, indicating a sufficient nutrient
supply. Iron concentrations in the biomass were in
line with the average Fe contents of plants
(50200 mg kg1), although the total iron content
may not serve as the best criterion for the Fe status
of plant biomass (Bergmann, 1992). Ca and Mn concentrations were similar in 2012 and 2013, accompanied by constant nutrient removal and higher
nutrient use efficiency due to increased biomass
growth for Ca and constant nutrient use efficiency
and an increased removal in the case of Mn. This
indicates that for these elements, the dilution effect
does not apply, but neither was optimum supply
attained. Sodium concentrations and removals were
constant over both years, indicating that these elements were not limiting.

Treatment effects
Macronutrients: nitrogen, phosphorus, potassium,
sulphur, magnesium and calcium
In general, removal and concentration of N in the biomass was not influenced by any carbon amendment,
compared to the control plots, indicating that either
the carbon amendments had no N-limiting effect, as
was reported from other studies with Miscanthus straw
(Eiland et al., 2001) or sugar beet/wheat straw hydrochar (Gajic and Koch, 2012; Bargmann et al., 2014),
or more N that could be immobilized was added with
the slurry. Nevertheless, we observed a grass biomass

2015 John Wiley & Sons Ltd. Grass and Forage Science

13

growth reduction in the hydrochar-amended plots in

2011, the year of application, that was likely caused
by initial N-immobilization or phytotoxic effects (Bargmann et al., 2013; Busch et al., 2013). However, as the
results presented here show, this short-term effect was
outbalanced in the following years. Higher biomass N
concentrations due to biochar + N-fertilizer application
to soil, as found in incubation experiments (Chan
et al., 2008; Van Zwieten et al., 2010; Schimmelpfennig et al., 2014), were not observed, likely because the
biochar was not directly mixed into the soil matrix
due to top dressing. Moreover, biochars0 beneficial role
in soil nitrogen cycling might not be the decisive factor in soils with a naturally high nitrifier activity, as in
the grassland used here (Kammann et al., 1998; DeLuca et al., 2006).
Potassium concentrations were increased in all
carbon-amended plots, and correlated with the initial
K concentrations of the materials, indicating a fertilization effect. Removal of K was only higher in
hydrochar- and biochar-amended plots, compared to
the control (Figure 3). The difference was made up
mostly by the higher share of forbs in these plots,
confirming the promotion of forb over grass biomass
growth by the carbon amendments (Figures 1 and
5a). Potassium has been found to be easily leached
from biochar, thereby providing fertilizer to plants
(Gaskin et al., 2010; Silber et al., 2010; Yao et al.,
2010; Angst and Sohi, 2013; Wagner and
Kaupenjohann, 2014). Likewise, K from hydrochar is
reportedly plant available (Gajic and Koch, 2012)
and water soluble (Wagner and Kaupenjohann,
2014). A long-term K fertilization effect due to carbon amendment has been described as unlikely
(Angst and Sohi, 2013), but has also been found in
a natural grass system (Van de Voorde et al., 2013).
Besides the direct fertilization effect, the sorption of
K from slurry by negatively charged functional
groups on the biochar/hydrochar surface could also
be a reason for improved K availability in our experiment (Sevilla and Fuertes, 2009; Mukherjee et al.,
2011).
Both Ca and Mg contents were concentrated by
the hydrothermal carbonization and pyrolysis process,
compared to the feedstock material; nevertheless, the
nutrient amounts applied with all carbon amendments
were quite low, but were highest with hydrochar
amendment (78 g m2) (Table 3). Similar Ca and Mg
concentrations of the biomass from carbon-amended
plots, combined with a higher nutrient removal, are
likely due to the overall higher share of forbs in the
carbon-amended plots in the total biomass for the
2 years, compared to the control (Figures 1 and 5a).
The higher Ca and Mg removal in the hydrochar plots,
compared to the control plots, indicates that Ca and

14

S. Schimmelpfennig et al.

Mg from hydrochar were available to plants, especially

to forbs (Figure 5a). The influence of hydrochar on
nutrient uptake or concentrations in plants is often
masked by a reduced plant growth due to N-limitation
or toxic effects (Gajic and Koch, 2012; Busch et al.,
2013; Jandl et al., 2013; Wagner and Kaupenjohann,
2014). Growth reduction by N-limitation was not
observed in our experiment; nevertheless, N supply
was rather low, and a possible fertilizer effect of Ca
and Mg may have been masked by suboptimal N
supply.

Micronutrients: iron, copper, zinc, manganese, sodium

and chloride
Iron, Cu Zn and Cl concentrations in plant biomass
were not influenced by any of the carbon amendments, compared to the control. Concentrations of Fe
in the biomass suggest sufficient Fe supply in both
years and all treatment plots. Surprisingly, the Fe concentrations of the carbon amendments were not
reflected in the biomass from the corresponding plots
(Table 3, Figure 2 a and b). This indicates that the carbon amendments were either not degraded enough to
release the Fe bound in the material, or that if Fe
became soluble that it was taken up during the first
year after application or bound in organo-mineral
complexes. Bioavailability of Fe from plant residues
was reported by others to be highest within the first
year of amendment, especially if decomposition of the
residues was enhanced by earthworms, fungi or composting (Palviainen et al., 2004; Maqueda et al., 2011;
Bityutskii et al., 2012).
The Cu results indicate that although additional
Cu was introduced with all carbon amendments, the
applied surplus was apparently not available to
plants. Elevated leaf concentrations of Cu have been
reported previously but only from biochar produced
from Cu-contaminated wood waste with a concentration of 221 g kg1 (which is a thousand-fold higher
than in biochar from non-contaminated biomass),
indicating that Cu from biochar itself may become
available to plants at some stage (Lucchini et al.,
2014). Presumably, in our experiment, Cu is bound
to the organic carbon fraction of the soil, in a form
that is not readily plant available (Sims, 1986; Beesley et al., 2010).
Zinc accumulated in the carbon amendments due
to the carbonization processes. Nevertheless, Zn did
not accumulate in the biomass grown on carbonsupplemented plots, indicating that it was not plant
available.
Hydrochar and biochar did not influence plant biomass Mn concentrations or uptake, although substantial amounts of Mn were added with both

amendments to the soil, especially with biochar

(Table 3). In contrast, feedstock amendment significantly increased Mn concentrations and uptake by the
plants. However, Mn toxicity was not observed and
has only been reported for plant Mn concentrations
>1000 mg kg1, although this also depends on the
plant species, and soil pH (Bergmann, 1992). It seems
likely that the provision of easily decomposable
organic matter such as Miscanthus straw caused Mn
complexes in the soil to change from less soluble
forms to more plant-available forms, likely by participating in redox reactions, dissolving Mn oxides (Stone
and Morgan, 1984; Shuman, 1988).
It is assumed, as ongoing bioturbation will foster
degradation and merging of hydrochar and biochar
with the soil matrix, that either Mn bound in these
materials will become plant available and/or hydrochar and biochar may participate in soil redox reactions, as found by Graber et al. (2014).
The higher Na concentrations and uptake by biomass of the control plots compared to all other treatment plots was remarkable, as Na added with the
carbon amendments was in very small amounts. Considering the additional K, Ca and Mg applied with the
carbon amendments, an ion antagonism in the feedstock, hydrochar and biochar plots could likely explain
these differences, leading to a reduced uptake of Na.
Nevertheless, the range of Na concentrations in the
harvested biomass indicates neither Na deficiency nor
excess. Generally, Na deficiency is rarely reported for
grassland, and likewise, concentrations found here are
well below critical values for excess supply (Bergmann, 1992).
Chlorine was neither added in considerable
amounts with the carbon amendments, nor did the
carbon amendments influence the soil0 s Cl availability
by complexation with, e.g., Na. Thus, the effect of carbon amendments on Cl availability was negligible in
the grassland under study.

Fodder quality
The fodder quality of the plant biomass harvested
from all plots under study, with respect to micro- and
macronutrients, meets (P, S, Cu and Zn) or even
exceeds the recommended intake requirements for
dairy cows, especially in terms of the base cations K,
Ca and Mg as well as Fe, Mn and Cl (Table 4), with
no significant positive or negative effects of carbon
amendments. The concentration of K in the biomass
of all treatments exceeded the recommended intake
by 70% on average, indicating that K supply for animal nutrition was more than sufficient, independent
of carbon amendment. Excessive K intake with biomass feed can disturb Mg resorption of ruminants,

2015 John Wiley & Sons Ltd. Grass and Forage Science

Carbon amendment to temperate grassland

leading to grass tetany in the worst case (Ter

orde,
1997). Nevertheless, supplementary Mg is only
essential if K concentrations increase to 35 g kg1
dry biomass or more (Kessler, 2001), a situation not
reached in our experiment. Magnesium concentrations in our biomass were up to 94% higher than
the recommended intake, independent of carbon
amendment, accompanied by an increase in Ca contents of up to 60%. High Ca concentrations in biomass can reduce fodder quality if Mg, P or Vitamin
D supplies are insufficient (Ter
orde, 1997). Commonly, a K/(Ca+Mg) ratio 22 is regarded as an
indicator for low nutrient antagonism and an adequate nutritive balance (Reid and Horvath, 1980).
This threshold was met by all of our biomass with an
average ratio of 135. In this context, high Mg and
Ca concentrations, as found here, can be considered
positive. Furthermore, the Ca:P ratio of biomass can
serve as an indicator for an optimal uptake of Ca by
ruminants. Best Ca uptake rates by ruminants are
reported for biomass with a Ca:P ratio of 2 (Ter
orde,
1997). The mean Ca:P ratio of our biomass was
rather high (2.9) and was highest in biomass from
hydrochar-amended plots. Nevertheless, if requirements concerning P supply are met, the ability of
ruminants to adapt to fluctuations in Ca supply is
high (Flachowsky et al., 2001; McDonald, 2002).
Thus, rather high Ca contents as observed here are
not considered harmful for animal nutrition. Moreover, hydrochar and biochar application together
with an additional P-source such as slurry may be an
option to increase the fodder quality of biomass
grown on such char-amended soil (Sarkhot et al.,
2013). Iron contents in biomass from grazing land
often exceed the requirements for Fe intake of ruminants, as also found here. Tolerance levels for iron
are reportedly as high as 500 mg kg1, which was
not reached by the biomass in any of the treatments,
with a mean Fe concentration of 1788 mg kg1
(Table 4) (Flachowsky et al., 2001).
Negative impacts on animal health from Cl in biomass have not been reported. Likewise, adverse
effects due to Mn intake have only been observed
for an intake 100-fold higher than the concentrations
measured in our treatments (Flachowsky et al.,
2001).
The minimal requirement of the daily intake was
met by the biomass from all treatment plots for all
nutrients except Na. This is also in accordance with
the long-term observations of German grassland, as Na
is a micronutrient for plants but a macronutrient for
animals (Whitehead, 2000). Thus, additional supply of
Na, for example by providing salt blocks, may be necessary on many grasslands. Carbon amendment did
not improve the Na supply for plants.

2015 John Wiley & Sons Ltd. Grass and Forage Science

15

Generally, the nutrient concentrations of the biomass from our experiment are in good agreement with
the reported long-term observations of grasslands in
Germany, with no significant differences found
between the treatments and the DLG values.

Conclusion
Our results indicate that uncarbonized and carbonized
Miscanthus x giganteus materials had neither positive
nor adverse effects on biomass production in the second and third year after application. The main limitation to plant growth at the experimental site in all
treatment plots was probably N, possibly masking other
nutrient effects. Interactions of the carbon amendments with slurry did not occur, neither improving nor
worsening the nutrient use efficiency of slurry amendment. Although total biomass growth was not affected
by the carbon amendments, biochar led to a shift from
grasses to forbs, leading to a total yield enriched in
most nutrients. Both hydrochar and biochar led to
increased K concentrations in the biomass over the
2 years, with a positive correlation to the initial K contents of the carbon amendments. Likewise, K removal
by biomass was improved in hydro- and biochar plots,
accompanied by a decreased removal of Na, indicating
an ion antagonism. This leads to the assumption that
even 2 years after application, hydrochar and biochar
exhibited a K fertilization effect. Additionally, Ca
removal by biomass, especially forbs, was increased by
all carbon amendments, indicating, together with Mg
in hydrochar plots, plant-available Ca and Mg components in the carbon amendments.
Heavy metals (Fe, Cu and Zn) were concentrated
in hydrochar and biochar due to the carbonization
processes, but did not accumulate in plant biomass
accordingly. Feedstock application led to an increased
Mn concentration and its removal in the plant biomass, indicating participation of the feedstock material
in redox reactions in soil. In terms of plant and animal
health, application of carbon amendments did not present major risks. Recommended intakes were met or
exceeded for all nutrients except Na.

Acknowledgments
We thank Ms. Anja Fl
orke from the Hessian Federal
Laboratory for analysis of the plant samples and the
Hessian Agency for the Environment and Geology for
funding the project. We acknowledge the assistance of
Birte Lenz and Anastasija Gajdasch in terms of the elemental analysis and preparation of the samples and
thank Christian Eckhardt for logistical help during biomass harvest and differentiation. All authors declare
no conflict of interest.

16

S. Schimmelpfennig et al.

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